Integrated multi-omics analysis of muscle identifies H3K4me3 epigenetic regulation of growth traits in pacific white shrimp (Litopenaeus vannamei)

The Pacific white shrimp ( Litopenaeus vannamei ) is the predominant aquaculture species worldwide, and China has the highest production value in its cultivation. Growth traits are widely acknowledged as the most critical economic characteristics in shrimp farming. Genome-wide association study (GWAS) is a tool to dissect the genetic basis of the target traits. Histone methylation, particularly trimethylated H3 lysine 4 (H3K4me3), plays a pivotal role as a posttranslational modification that regulates gene expression by influencing chromatin compaction. In this research, we conducted a genome-wide association study (GWAS) on L. vannamei . Through this in-depth analysis, we successfully identified several genes associated with fast-growth traits. Notably, a histone methyltransferase (HMT) gene presented significantly different expression levels between shrimp with distinct growth phenotypes. To gain a more comprehensive understanding of the histone modification mechanisms underlying these growth disparities, we employed CUT & Tag analysis. A total of 165 differential peaks (DPs) were identified, comprising 75 DPs related to gain (gain DPs) and 90 DPs related to loss (loss DPs). Gene annotation was performed on these classified DPs, and a total of 146 differential peaks genes (DPGs) were found. Among them, 65 were gained DPGs, and 81 were lost DPGs, which were involved in pathways such as glycolysis/gluconeogenesis, carbon metabolism, and nitrogen metabolism. By integrating the CUT & Tag results with our previous RNA-seq data, we identified 18 differentially expressed genes (DEGs) that were associated with H3K4me3 modification. Specifically, 12 DEGs with loss DPs (down-regulated) and 6 DEGs with gain DPs (up-regulated). Key genes such as triose-phosphate isomerase ( TPI ), 4-α-glucanotransferase ( 4αGTs ), glucose-6-phosphate isomerase ( GPI ), and purine nucleoside phosphorylase ( PNPase ) were also identified. The presence of these genes strongly suggests their crucial contributions to nutrient absorption and cell growth. This study not only successfully identified multiple functional genes related to growth traits through GWAS but also comprehensively investigated the role of histone modification in regulating shrimp growth. By integrating CUT & Tag analysis with transcriptome data analysis, our research offers initial yet valuable insight into the H3K4me3 modification regulatory mechanisms governing growth performance in L. vannamei . • kmt2d (LOC113822061) is identified as a key gene associated with shrimp growth trait. • H3K4me3 influence the shrimp carbon and nitrogen metabolism pathways. • Expression of TPI, 4αGTs, GPI and PNPase were associated with H3K4me3 modification.